The Prevalence, Epidemiological, and Molecular Characterization of Methicillin-Resistant Staphylococcus aureus (MRSA) in Macau (2017–2022)

Macau, recognized as a global tourism hub and the world’s most densely populated region, provides a unique environment conducive to methicillin-resistant Staphylococcus aureus (MRSA) transmission in healthcare and community settings, posing a significant public health concern both locally and globally. The epidemiology and molecular characteristics of MRSA in the distinct city of Macau remain largely unelucidated. This five-year longitudinal study (2017–2022) examined the local prevalence and molecular typing of MRSA in Macau, with future MRSA type distribution predicted through ARIMA modeling. We subsequently analyzed the epidemiological characteristics of MRSA, including specimen source, clinical department, collection year, season, patient age, sex, and the annual number of tourists. Comprehensive antibiotic resistance profiles of the strains were also assessed. Of 504 clinically isolated S. aureus strains, 183 (36.3%) were identified as MRSA by the cefoxitin disk diffusion method and validated through multi-locus sequence typing (MLST). The MRSA detection rate showed an upward trend, increasing from 30.1% in 2017 to 45.7% in 2022. SCCmec type IV was predominant (28.9%), followed by types II (25.4%), III (22.1%), and V (22.1%). The primary sources of MRSA isolates were sputum (39.2%) and secretions (25.6%). Older age emerged as a risk factor for MRSA infection, whereas no significant associations were found with seasonal variations, gender, or the annual number of tourists. Despite displaying universal resistance to cefoxitin, oxacillin, and benzylpenicillin, MRSA isolates in Macau remained fully sensitive to vancomycin, tigecycline, quinupristin, nitrofurantoin, and linezolid. Continuous surveillance and analysis of MRSA distribution in Macau could provide invaluable insights for the effective management of MRSA prevention and control measures within healthcare settings.


Introduction
Methicillin-resistant Staphylococcus aureus (MRSA) strains have spread rapidly worldwide since the 1990s.The increasing prevalence of MRSA and continual development of drug resistance mechanisms have posed substantial challenges for the clinical management of infections [1,2].MRSA is highly pathogenic, capable of causing severe progressive and necrotizing diseases, including bacteremia, sepsis, and toxic shock syndrome [3].According to the monitoring report from the China Antimicrobial Surveillance Network (CHINET), the detection rate of Staphylococcus aureus (SA), particularly MRSA, ranks first among Grampositive bacteria [4].It is considered one of the most severe pathogenic bacteria in clinical settings.In recent years, with the widespread use of antibiotics such as methicillin, the resistance of SA, especially MRSA, has gradually increased, leading to a global prevalence

Materials and Methods
Brief methods are summarized below, and the details of methodology can be found in the Supplementary Material/Methods section.

Sample Collection and Strain Isolation
Kiang Wu Hospital is one of the largest hospitals in Macau with a total of 736 beds and is equipped with 19 clinical departments, including internal medicine, surgery, obstetrics and gynecology, and laboratory medicine.In 2022, the emergency department treated 1.37 million patients, and there were 28,300 discharges (http://www.kwh.org.mo/kwh/,accessed on 1 December 2023).Samples in this study were selected from all patients who sought medical care at Kiang Wu Hospital, with an age range from 7 days to 101 years between September 2017 and April 2022.S. aureus isolates were recovered from inpatients and outpatients who had cough, fever, skin abscess, and other infection-related clinical symptoms using sterile swabs or other appropriate collection tools from sites relevant to S. aureus colonization or infection, such as nasal passages, wounds, or skin lesions.A total of 504 non-duplicate strains of S. aureus were collected and isolated from the Departments of Respiratory Medicine, General Surgery, Dermatology, Neurology, and others.Among them, 276 were males, 184 were females, and 47 cases had unrecorded gender information.Various sample types were collected from patients, including pus, urine, blood, sputum, secretions, and ascites.All strains were identified using the VITEK-2 automated microbial identification system (bioMérieux, Lyon, France).To confirm whether the isolated strains were MSSA or MRSA, multi-locus sequence typing (MLST) was conducted by randomly selected 2-3 isolates from each survey period.The study protocols were approved by the Institutional Review Board (IRB) of Kiang Wu Hospital (Protocol ID#: 2018-004).

SCCmec Typing
The SCCmec typing of MRSA isolates was performed using the multiplex PCR method [27].All oligonucleotide primers used in this study were synthesized by Sangon Biotech (Shanghai, China).SCCmec types I-V were identified based on the combination of the cassette chromosome recombinase (ccr) type and mec class.The primers and PCR programs for amplification of the relevant genes were listed in Supplementary Table S1.After the reaction, a 6× DNA loading buffer was added to the PCR products, and 20 µL of the mixture was loaded onto a 1.2% agarose gel for electrophoresis at 110 V for 40 min.The gel was visualized, and images were captured using a UV gel imaging system.S. aureus ATCC43300, ATCC25923, ATCC33591, and ATCC49775 were used as quality control strains.

Sequence Analysis
Amplified gel bands were excised under UV light using a cutter and purified with the Gene ALL Gel Purification Kit per the manufacturer's protocol.Purified samples were sequenced by Sangon Biotech (Shanghai, China).The nucleotide sequences were aligned with Clustal W using the msa R package (v1.30.1).A phylogenetic tree was then constructed using neighbor-joining (NJ) methods using the ape (v5.7-1)R package and visualized by the ggtree (v3.6.2) package in R.

Epidemilogical Analysis
The occurrence of MRSA was stratified by specimen source, clinical department, collection year, season, patient age, and sex, and the differences between these factors were compared using Chi-square analysis.Tourism data on annual tourists in Macau from 2017 to 2022 were retrieved from the Macao Government Tourism Office (https://dataplus.macaotourism.gov.mo/,accessed on 21 October 2023).The associations between MRSA occurrence and age and the annual number of international travelers were analyzed using Pearson's correlation.

Autoregressive Integrated Moving Average (ARIMA) Modeling
The ARIMA modeling was employed to forecast future MRSA prevalence trends in Macau using the R packages, tseries (v0.10-53) and forecast (v8.21.1).The model was fitted to the past five years of MRSA typing data collected in this study from 2017 to 2022.

Antimicrobial Susceptibility Testing
All clinical specimens for isolation and cultivation were processed according to the National Operating Procedures for Clinical Laboratory Testing.Antimicrobial susceptibility of the 504 strains of S. aureus was tested against 16 drugs using VITEK-2 AST cards (bioMérieux, France) based on the manufacturer's standard protocol.The tested antibiotics were: cefoxitin, benzylpenicillin, oxacillin, linezolid, gentamicin, ciprofloxacin, levofloxacin, moxifloxacin, erythromycin, clindamycin, quinupristin, vancomycin, tetracycline, tigecycline, nitrofurantoin, and rifampicin.The minimum inhibitory concentration (MIC) breakpoints of antimicrobials for S. aureus using VITEK-2 COMPACT system can be referred to in Supplementary Table S2.The criteria for antimicrobial susceptibility determination and quality control were based on the 2017 Clinical and Laboratory Standards Institute (CLSI) guidelines.The MRSA phenotype was determined using the cefoxitin disk diffusion method [28].Further details can be found in the Supplementary Material/Methods section.

Statistical Analysis
All statistical analyses were performed in R (v4.2.1) unless otherwise specified.Continuous data are expressed as mean ± standard deviation (SD) or median and interquartile range (IQR) based on distribution.The categorical variables are shown as value (%).Chi-squared tests were performed for the comparison of categorical variables.Person's correlation analysis was performed to analyze the associations between MRSA occurrence and the continuous variables.The proportions were compared using two-proportional z-tests.p < 0.05 was considered statistically significant.Data were visualized using R packages of ggplot2 (v3.4.2), seqinr (v4.2-30), pheatmap (v1.0.12), and ggtree.

Overview of the Study Design
The study design is outlined in Figure 1.During the period from 2017 to 2022, S. aureus strains were collected annually from September to the following April at Kiang Wu Hospital, the main hospital in Macau.MRSA identification was done by cefoxitin disk diffusion and further confirmed by VITEK-2 microbiology analysis.The main SCCmec types (I-V) were identified using multiplex PCR and sequencing.The epidemiological characteristics of MRSA in Macau were then analyzed, including specimen source, clinical department, collection year, season, patient age, and sex.Subsequently, the comprehensive antibiotic resistance profiles of Macau MRSA strains were explored.diffusion and further confirmed by VITEK-2 microbiology analysis.The main SCCm types (I-V) were identified using multiplex PCR and sequencing.The epidemiologi characteristics of MRSA in Macau were then analyzed, including specimen source, clini department, collection year, season, patient age, and sex.Subsequently, the comprehe sive antibiotic resistance profiles of Macau MRSA strains were explored.

SCCmec (I~V) Gene Detection
Electrophoresis and Nanodrop quantification showed high-quality bacterial DN extracted from MRSA strains and quality control strains.Agarose gel electrophoresis PCR products for the eight candidate reference genes displayed single bands at expect sizes (Figure S1A).The phylogenetic relationships of the 8 SCCmec genes were assess by generating a phylogenetic tree based on DNA sequences (Figure S1B).Sequence alig ment and a similarity heatmap demonstrated high sequence similarity among the 8 gen (Figure S1C,D).

Multi-Locus Sequence Typing of S. aureus Isolates
The sequencing data were uploaded to the PubMLST database for online analys Each S. aureus isolate was assigned a sequence type (ST) and clonal complex (CC) bas on the combination of 7 housekeeping genes, known as the allelic profile (Table 1).Pre ous studies [29][30][31][32][33][34] have confirmed that ST5, ST7, ST15, ST30, and ST398 are MSSA, wh ST45 and ST59 are MRSA, which is consistent with the results obtained from the cefoxi

SCCmec (I~V) Gene Detection
Electrophoresis and Nanodrop quantification showed high-quality bacterial DNA extracted from MRSA strains and quality control strains.Agarose gel electrophoresis of PCR products for the eight candidate reference genes displayed single bands at expected sizes (Figure S1A).The phylogenetic relationships of the 8 SCCmec genes were assessed by generating a phylogenetic tree based on DNA sequences (Figure S1B).Sequence alignment and a similarity heatmap demonstrated high sequence similarity among the 8 genes (Figure S1C,D).

Multi-Locus Sequence Typing of S. aureus Isolates
The sequencing data were uploaded to the PubMLST database for online analysis.Each S. aureus isolate was assigned a sequence type (ST) and clonal complex (CC) based on the combination of 7 housekeeping genes, known as the allelic profile (Table 1).Previous studies [29][30][31][32][33][34] have confirmed that ST5, ST7, ST15, ST30, and ST398 are MSSA, while ST45 and ST59 are MRSA, which is consistent with the results obtained from the cefoxitin disk diffusion method for MRSA identification.Subsequently, a dendrogram was constructed to conduct evolutionary analysis and assess the genetic relatedness among these strains (Figure 2).disk diffusion method for MRSA identification.Subsequently, a dendrogram was constructed to conduct evolutionary analysis and assess the genetic relatedness among these strains (Figure 2).

Molecular Typing of MRSA Strains in Macau
Using SCCmec typing, 8 types and subtypes (I, II, III, IVa, IVb, IVc, IVd, V) were identified among the 183 MRSA isolates.Comparison of typing by survey period (Figure S2A-E) revealed that the predominant MRSA type varied annually.However, from the figures, it can be observed that Type II, III, IV, and V are relatively more prevalent, with Type I constituting a relatively small proportion.The results from the five survey periods reflect inconsistent patterns of predominant types, indicating that the MRSA typing landscape in Macau is dynamically changing.Overall, type IV was the most predominant (28.8%), accounting for approximately one-sixth of all MRSA isolates (Figure S2F), followed by III (25.4%),III (22.0%), and V (22.0%).Two isolates were non-typable (NT) by SCCmec.

Epidemilogical Characteristics of MRSA Strains in Macau
During the study period from 2017 to 2022, a total of 504 strains of S. aureus were identified (Table 2), of which 183 were MRSA (36.3%) and 321 were MSSA (63.7%).The highest number of MRSA cases was detected in 2021-2022 (58 strains), with the highest detection rate of MRSA in 2019-2020 (47.9%, 23/48).The MRSA detection rates of other years were 30.1% (2017-2018), 33.3% (2018-2019), 30.0%(2020-2021), and 45.7% (2021-2022), respectively.Chi-square analysis revealed significant differences in MRSA detection rates between years (p = 0.018) and in MRSA detection rates between different years (Table 2).Due to the peak tourism season in Macau during the Winter and Spring, MRSA occurrence tends to be relatively higher during this period, but seasonal differences were not significant (p = 0.13), as shown in Table 2.
Table 3 compares the molecular typing of MRSA infections between inpatient and outpatient groups.The data demonstrate that SCCmec III was significantly more prevalent among inpatients (8.9%) compared to the outpatient group (2.4%), with a significant difference of p = 0.028.Conversely, there are no statistically significant differences in the distribution of SCCmec I, II, IV, and V between inpatients and outpatients (p > 0.05).These findings suggest that SCCmec III MRSA may be more closely associated with nosocomial infections in Macau, whereas the other SCCmec types appear to play a relatively balanced role in the transmission of MRSA among both inpatient and outpatient settings.Differences between inpatients and outpatients were analyzed using Chi-square tests (categorical data).
The proportions between the two groups were analyzed using the two-proportion z-test.p < 0.05 was statistically significant.
MRSA phenotypes over time shows Types IV, II, III, and V as predominant in Macau, with Type III being most stable (Figure 4B).We further used ARIMA modeling to predict MRSA subtype distribution in Macau for 2022-2023 (Figure 5A-E).The forecasts show type III has maintained an increasing trend, and is expected to remain a predominant type in 2022-2023.Additionally, the predicted proportion of type II exceeds 10%, indicating that this MRSA type will also remain prevalent.Having been a Portuguese colony for over 400 years, Macau has retained some European lifestyles.Simultaneously, it serves as an international tourist and gambling hub, attracting a multitude of visitors from various regions worldwide with over a million visitors annually (Figure 4A).Reflecting this, MRSA molecular epidemiology in Macau is diverse (Figure S2A-F).As depicted in Figure 4B, the detection rate of MRSA in Macau remained over 30% from 2017 to 2022, with a notable upward trend from 2017 to 2019.MRSA detection rates declined in 2020-2021, potentially due to reduced tourism during the COVID-19 pandemic.In the post-pandemic period of 2021-2022, MRSA detection rates in Macau rose again to 46%, suggesting a potential association between MRSA incidence and tourist numbers, though not statistically significant (p = 0.47).Distribution of MRSA phenotypes over time shows Types IV, II, III, and V as predominant in Macau, with Type III being most stable (Figure 4B).We further used ARIMA modeling to predict MRSA subtype distribution in Macau for 2022-2023 (Figure 5A-E).The forecasts show type III has maintained an increasing trend, and is expected to remain a predominant type in 2022-2023.Additionally, the predicted proportion of type II exceeds 10%, indicating that this MRSA type will also remain prevalent.

Drug Resistance Characteristics of MRSA in Macau
All 504 S. aureus isolates were examined for antimicrobial susceptibility; their antimicrobial resistance profiles are shown in Supplementary Table S3, and the relationship between MRSA SCCmec typing and drug resistance is shown in Figure 6.All SCCmec types I-V were resistant to Cefoxitin, Oxacillin, and Benzylpenicillin but sensitive to Vancomycin, Tigecycline, Quinupristin, Nitrofurantoin, and Linezolid.Resistance to partial antimicrobial agents was observed among the majority of isolates.Specifically, 69.4% of isolates demonstrated resistance to erythromycin.Clindamycin resistance was observed in 63.9% of isolates, while 51.7% showed resistance to levofloxacin, and 55.3% to ciprofloxacin.Resistance to moxifloxacin was demonstrated in 37.2% of isolates, and resistance to gentamicin and tetracycline was observed in 29.1% and 27.2%, respectively.Statistical tests revealed that resistance to Cefoxitin, Benzylpenicillin, Oxacillin, Gentamicin, Ciprofloxacin, Levofloxacin, Moxifloxacin, Erytromycin, and Clindamycin were significantly associated with MRSA infection (Table 4), with statistical significance (p < 0.05).

Drug Resistance Characteristics of MRSA in Macau
All 504 S. aureus isolates were examined for antimicrobial susceptibility; their antimicrobial resistance profiles are shown in Supplementary Table S3, and the relationship between MRSA SCCmec typing and drug resistance is shown in Figure 6.All SCCmec types I-V were resistant to Cefoxitin, Oxacillin, and Benzylpenicillin but sensitive to Vancomycin, Tigecycline, Quinupristin, Nitrofurantoin, and Linezolid.Resistance to partial antimicrobial agents was observed among the majority of isolates.Specifically, 69.4% of isolates demonstrated resistance to erythromycin.Clindamycin resistance was observed in 63.9% of isolates, while 51.7% showed resistance to levofloxacin, and 55.3% to ciprofloxacin.Resistance to moxifloxacin was demonstrated in 37.2% of isolates, and resistance to gentamicin and tetracycline was observed in 29.1% and 27.2%, respectively.Statistical tests revealed that resistance to Cefoxitin, Benzylpenicillin, Oxacillin, Gentamicin, Ciprofloxacin, Levofloxacin, Moxifloxacin, Erytromycin, and Clindamycin were significantly associated with MRSA infection (Table 4), with statistical significance (p < 0.05).

Discussion
MRSA is a major cause of both hospital-acquired and community-acquired infections [35,36].MRSA exhibits multidrug resistance, including resistance to β-lactam antibiotics, and high virulence, sometimes leading to fatal outcomes [37,38].Due to its pathogenicity and pan-resistance, MRSA poses a considerable public health threat, especially in highly populated Macau with high volumes of international travel and a mixed Western and Eastern cultural heritage.To our best knowledge, this is the first comprehensive investigation of the uniqueness of MRSA in the clinical settings of Macau.
We employed a standardized annual sampling window from September through the following April for several reasons.First, winter and spring in Macau coincide with seasonal peaks in colds and influenza, corresponding to a heightened risk of hospital-acquired infections, as indicated by our preliminary data.Second, in Macau, tourism significantly fluctuates throughout the year, with peak seasons typically occurring in the months included in our collection period.The increase in tourist numbers may correlate with a rise in the spread of infectious diseases, including S. aureus, due to higher human traffic and density.This aspect was carefully considered, as it could introduce a variable that may affect the prevalence and diversity of the strains.Third, by maintaining a consistent collection window each year, we aimed to minimize variables that could potentially bias our data, thus ensuring comparability across the years within similar seasonal and tourist influx conditions.Finally, the sampling period has been approved by the hospital's infection management department, with a focus on addressing the risks associated with peak tourist seasons.
The MRSA detection rate in Macau hospitals increased significantly from 2017 to 2022, rising from 30.0% to 47.9%.This surge surpassed the average MRSA detection rate in tertiary hospitals across Mainland China [14], indicating a notably higher prevalence of MRSA in the region and calling for heightened vigilance from the Macau Health Bureau.SCCmec is a mobile genetic element carrying the mecA gene, utilized for MRSA typing due to its essential components, including mec complexes, ccr complexes, and the J region.Types I, II, and III are predominantly associated with hospital-acquired MRSA (HA-MRSA), while types IV and V are commonly linked to community-acquired MRSA (CA-MRSA).This study, for the first time, conducted a study on the most common SCCmec types I to V in Macau's MRSA strains.The findings indicated the detection of types II to V, with type IV being predominant, followed by types II, III, and V, excluding type I.This diversity in the SCCmec typing of Macau's MRSA strains indirectly confirmed the coexistence of both CA-MRSA and HA-MRSA in the region.Previous data have indicated that the predominant strains in Asia are types II, III, and IV [6,14,39], and a multicenter longitudinal study in 2022 showed that epidemic typing of MRSA was ST59-t437-IV (14.9%),ST239-t030-III (6.4%) and ST5-t2460-II (6.0%) in Mainland China [40].The diverse typing observed in Macau may be correlated with its geographical location.Furthermore, the influx of tourists from various parts of the world to Macau, including a significant number from Mainland China, Hong Kong, and Taiwan (data from dataplus.macaotourism.gov.mo), could contribute to this diversity.Projections from the ARIMA model suggest an upcoming decline in type IV prevalence, which might be associated with the prevalence of type II MRSA in the Guangdong province, a nearby region of Macau [40].
In terms of epidemiological characteristics, we found that age is positively associated with MRSA occurrence in Macau, with adults over 60 at a higher risk.Older adults tend to have weaker immunity and infection defenses [41].Over 30% of MRSA cases originated from sputum, then by secretions and pus, aligning with prior reports [42,43].This highlights the need to strengthen prevention, enhance sputum surveillance, and monitor bacterial strains in patients with lower respiratory tract infections.
Seasonal variation in S. aureus infections is controversial.Some studies have demonstrated surges in MRSA during warmer months and autumn in hospitals [44] and community [45] in temperate and tropical climates.However, we did not observe a significant correlation between seasonal fluctuations and MRSA infection in Macau.Several factors may account for this discrepancy.Macau's unique subtropical climate with minimal temperature variations could mitigate any seasonal impact on MRSA.Increased international tourism and travel in Macau may introduce exogenous MRSA year-round, masking seasonal effects.Moreover, the persistent high density of the population in Macau could sustain endemic MRSA transmission, overriding seasonal factors.Further investigation is warranted to elucidate the reasons for the lack of seasonal variation in Macau's distinctive setting.Elucidating the effects of climate, travel patterns, and population factors could better explain MRSA epidemiology in Macau and similar subtropical cities.Additionally, we found universal susceptibility of Macau's MRSA strains to five common antibiotics: vancomycin, tigecycline, quinupristin, nitrofurantoin, and linezolid (100% each).Prior studies also noted 100% MRSA susceptibility to both linezolid and quinupristin [46].However, such broad universal susceptibility of MRSA to this panel of five antibiotics has not been previously documented.
Although our study provides an in-depth understanding of the trends and characteristics of MRSA in Macau, it is important to recognize certain limitations.The temporal scope (2017-2022) restricts a comprehensive grasp of long-term trends.Our ARIMA model predicted MRSA typing for the following year, but the unavailability of 2023 data (not yet disclosed by the Macau Health Bureau) hindered validation.Predominantly hospital-based samples may limit the generalizability of findings to community-acquired MRSA.Data constraints prevented exploration of influencing factors like patient travel histories and pathogen genetic variations.Future research should extend observation periods, include diverse community samples, and explore factors impacting MRSA epidemiology and antibiotic resistance in Macau's subtropical urban settings.

Conclusions
In summary, our study highlights a relatively higher MRSA detection rate (30.0-47.9%) in Macau compared to mainland China and Europe over the last five years (2017-2022), with the SCCmec type IV strain predominantly present, followed by types II, III, and V. Projections from the ARIMA model suggest an upcoming decline in type IV prevalence, accompanied by an increase in types II and III, indicating that the clone with SCCmec IV is probably correlated with the fitness of the clones with SCCmec II and III.Notably, despite seasonal fluctuations and international travel, hospital detection rates remained consistent.Moreover, sputum, secretions, and pus emerged as the most frequently detected specimens, with the respiratory department observing the highest MRSA incidence.Our findings underscore advanced age as a susceptibility factor for MRSA infections.Furthermore, our investigation revealed diverse antibiotic resistance profiles among MRSA strains in Macau, demonstrating universal sensitivity to vancomycin, tigecycline, quinupristin, nitrofurantoin, and linezolid, alongside complete resistance to cefoxitin, oxacillin, and benzylpenicillin.This comprehensive analysis highlights the unique epidemiological and resistance patterns of MRSA in Macau, emphasizing the significance of tailored, proactive measures for the effective management and control of this pathogen within the region.

Figure 1 .
Figure 1.The overall design of this study.

Figure 1 .
Figure 1.The overall design of this study.

Figure 3 .
Figure 3. MRSA detection rates in different specimens (A) and clinical departments (B).Note: for specimen (A), others contain abdominal drainage tube, articular matter, synovial fluid, skin, endotracheal tube, and body fluid.For clinical departments (B), others include Breast Clinic, Cardiothoracic Surgery, Diabetes Prevention and Control Center, Endocrinology, Intensive Care Unit, Laboratory, Nephrology, Obstetrics and Gynecology, Oncology, Ophthalmology, Otorhinolaryngology, Outreach Service Clinic, Rheumatology and Immunology, and Urology.

Figure 3 .
Figure 3. MRSA detection rates in different specimens (A) and clinical departments (B).Note: for specimen (A), others contain abdominal drainage tube, articular matter, synovial fluid, skin, endotracheal tube, and body fluid.For clinical departments (B), others include Breast Clinic, Cardiothoracic Surgery, Diabetes Prevention and Control Center, Endocrinology, Intensive Care Unit, Laboratory, Nephrology, Obstetrics and Gynecology, Oncology, Ophthalmology, Otorhinolaryngology, Outreach Service Clinic, Rheumatology and Immunology, and Urology.

Figure 4 .
Figure 4.The correlations between MRSA occurrence and the annual number of travels in Macau (A).Inbound visitor numbers and distribution by country and region in Macau (Source: https://dataplus.Macautourism.gov.mo/,accessed on 21 October 2023).(B) The distribution trend of different

Figure 4 .
Figure 4.The correlations between MRSA occurrence and the annual number of travels in Macau (A).Inbound visitor numbers and distribution by country and region in Macau (Source: https: //dataplus.Macautourism.gov.mo/,accessed on 21 October 2023).(B) The distribution trend of different SCCmec types.The thick blue line represents the change in MRSA rate over the years.Note: SCCmec IV (SCCmec IVa + SCCmec IVb + SCCmec IVc + SCCmec IVd).

Figure 6 .
Figure 6.Antimicrobial susceptibility testing of MRSA and MSSA.Red indicates susceptibility to antimicrobials, while blue represents resistance.The size of the circle is used to assess the consistency of drug susceptibility across different MRSA subtypes and MSSA strains.A value of 1 signifies consistent susceptibility to the antimicrobial, with smaller values indicating poorer consistency, suggesting uncertainty in the resistance pattern of the samples to that particular antimicrobial.MRSA: Methicillin-resistant Staphylococcus aureus; MSSA: Methicillin-susceptible Staphylococcus aureus.

Figure 6 .
Figure 6.Antimicrobial susceptibility testing of MRSA and MSSA.Red indicates susceptibility to antimicrobials, while blue represents resistance.The size of the circle is used to assess the consistency of drug susceptibility across different MRSA subtypes and MSSA strains.A value of 1 signifies consistent susceptibility to the antimicrobial, with smaller values indicating poorer consistency, suggesting uncertainty in the resistance pattern of the samples to that particular antimicrobial.MRSA: Methicillin-resistant Staphylococcus aureus; MSSA: Methicillin-susceptible Staphylococcus aureus.

Table 1 .
Allelic profile of each S. aureus isolate.

Table 2 .
Clinical characteristics of subjects stratified by methicillin susceptibility.
Data are mean ± standard deviation (SD) or median and interquartile range (IRQ) depending on the distribution.Differences between MSSA and MRSA were analyzed using either Student's t-tests (continuous data) or Mann-Whitney U tests (nonparametric continuous data) or Chi-square tests (categorical data).The proportions between the two groups were analyzed using the two-proportion z-test.p < 0.05 was statistically significant.MRSA: Methicillin-resistant Staphylococcus aureus; MSSA: Methicillin-susceptible Staphylococcus aureus.

Table 3 .
The patient characteristics stratified by inpatient or outpatient status.

Table 4 .
Antimicrobial susceptibility testing of S. aureus and MRSA.

Table 4 .
Antimicrobial susceptibility testing of S. aureus and MRSA.